Vlaams
Vlaams Diergeneeskundig
Diergeneeskundig Tijdschrift,
Tijdschrift, 2014,
2014, 83
83
Case report 255
255
Insidious progressive bone destruction in a dog surgically treated for otitis
media: follow-up by clinical examination and computed tomography
Progressieve botdestructie bij een hond die operatief werd behandeld voor otitis
media: follow-up via klinisch onderzoek en computertomografie
1
1
A. Furcas, 2I. M. Gielen, 1S. Vandenabeele, 2A. Van Caelenberg, 3L. Stessens, 1I. Polis,
1
H. de Rooster
Department of Medicine and Clinical Biology of Small Animals, Ghent University, Salisburylaan 133,
B-9820 Merelbeke, Belgium
2
Department of Veterinary Medical Imaging and Small Animal Orthopedics, Faculty of Veterinary
Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium
3
Department of Pathology, Ziekenhuis Oost Limburg (ZOL), Campus St. Jan, Schiepse Bos 6,
B-3600 Genk, Belgium.
[email protected]
A
BSTRACT
A 5.5-year-old Beagle was evaluated for abnormal swallowing and a head tilt of a two-weeks
duration. Inspection of the throat and external ear canal revealed an intact but abnormally
bulging eardrum. Computed tomographic (CT) examination showed a right-sided tympanic
bulla filled with soft-tissue density material, a partially lytic ventral wall and lysis of the petrosal
part of the temporal bone. Through ventral bulla osteotomy, sterile cholesterol granuloma and
cholesteatoma were diagnosed. The dog recovered but the head tilt re-appeared eight months
after surgery. A new CT scan showed expanded lysis of the tympanic wall and increased bone lysis
within the petrosal portion of the temporal bone. The owner elected for no further treatment.
Another two years later, a third CT scan was performed. Prominent intracranial involvement
was present. In contrast to the extent and the progression of the changes, the dog was clinically
stable.
SAMENVATTING
Een beagle van 5,5 jaar oud werd aangeboden omwille van klachten van abnormaal slikken en
een scheve kopstand die reeds twee weken aanwezig was. Inspectie van de keel werd uitgevoerd. Op
otoscopisch onderzoek werd een intact maar bolstaand trommelvlies aangetroffen. Op de beelden van
het computertomografisch (CT) onderzoek bleek de rechter bulla tympanica gevuld met materiaal met
een weke-delendensiteit, terwijl de ventrale bullawand deels lytisch was, evenals het pars petrosa van
het os temporale. De bulla werd benaderd via ventrale bulla osteotomie, waarbij een steriel cholesterol
granuloom en een cholesteatoma werden gediagnosticeerd. De hond herstelde, maar acht maanden na
de chirurgie trad opnieuw een scheve kopstand op. Een nieuwe CT-scan toonde uitbreiding van de lyse
van de bullawand en toegenomen lyse van het pars petrosum van het os temporale aan. De eigenaar
wenste geen nieuwe chirurgische interventie. Nog eens twee jaar later, werd de CT-scan herhaald.
Ditmaal was er een duidelijke intracraniale uitbreiding van het letsel zichtbaar. Niettegenstaande de
uitgebreidheid en de progressie van de letsels was de hond klinisch stabiel.
INTRODUCTION
In dogs, the prevalence of otitis media secondary
to otitis externa is relatively high. Nevertheless, many
cases are overlooked since the historical presentation
of chronic middle ear disease mimics the clinical signs
of therapy-resistant otitis externa (Gotthelf, 2004).
Both cholesterol granuloma (Fliegner et al., 2007)
and cholesteatoma (Lidl et al., 1991) can occur in
complicated otitis media cases in dogs. A cholesterol
granuloma is a slow-growing, non-neoplastic lesion
composed of cholesterol clefts surrounded by
256
granulation tissue, macrophages and foreign body
giant cells (Cox and Payne-Johnson, 1995; Banco et
al., 2014). There are only three cases reporting the
presence of a clinically relevant cholesterol granuloma
in the tympanic bulla in a dog (Cox and PayneJohnson, 1995; Fliegner et al., 2007; Riedinger et al.,
2012). In contrast, middle ear cholesteatoma seems
more common in dogs (Little et al., 1991, Hardie et
al., 2008, Greci et al., 2011). However, this condition
is probably also underdiagnosed. Cholesteatoma is
characterized by the presence of metabolically active
squamous epithelium surrounding lamellar sheets of
keratin debris (Little et al., 1991; Banco et al., 2014).
In a study on inflammatory middle ear disease in
dogs, cholesteatoma was diagnosed in as many as
11 % of the affected ears (Little et al., 1991).
The symptoms observed in dogs affected by
cholesterol granuloma or cholesteatoma depend
on the affected structures. Pain upon palpation of
the bulla or the temporomandibular joint and upon
opening of the mouth are symptoms, which are very
frequently observed in dogs with cholesteatoma
(Greci et al., 2011). Discomfort upon opening of the
mouth was also reported in two of the three cases of
canine middle ear cholesterol granuloma (Fliegner et
al., 2007; Riedinger et al., 2012). Also neurological
complaints, such as head tilt, facial paralysis and
ataxia are common in dogs with cholesteatoma
(Little et al., 1991; Hardie et al., 2008). In only one
of the three cases reporting a dog with cholesterol
granuloma, occasional and momentary facial palsy
and head tilt were reported by the owner, although
neurological examination at the time of presentation
to the veterinarian was unremarkable (Riedinger et
al., 2012).
Owing to its ability to detect subtle bony changes,
computed tomographic (CT) scanning is considered
the best imaging technique to identify cholesteatoma
in human patients who had not already had surgery
(Williams et al., 2003; De Foer et al., 2007). Also in
dogs, the CT finding of an expansile tympanic cavity
mass is highly suggestive for cholesteatoma (Hardie
et al., 2008; Travetti et al., 2010). There is recent
evidence that middle ear cholesterol granuloma in
dogs may also induce bone lysis (Fliegner et al., 2007;
Riedinger et al., 2012). In humans, magnetic resonance
imaging (MRI) is used for the differentiation between
aural cholesteatoma and cholesterol granuloma,
based on the difference in signal intensity on T1weighted images (Muzumdar et al., 2002). In dogs,
MRI findings have been described in one case of
cholesterol granuloma only (Riedinger et al., 2012).
In two case series on cholesteatoma in dogs, the use of
MRI has been reported (Sturges et al., 2006; Hardie et
al., 2008), but only recently, the MRI features in three
dogs with aural cholesteatoma have been described
(Harran et al., 2012; Schuenemann and Oechtering,
2012).
Medical therapy is not a viable treatment in
humans with cholesteatoma or cholesterol granuloma
Vlaams Diergeneeskundig Tijdschrift, 2014, 83
because expansion in close proximity to the ear is
potentially dangerous. However, following surgery,
a cholesteatoma persistence or recurrence rate as
high as 50% has been reported (Ajalloueyan, 2006).
Therefore, affected patients are routinely submitted
to regular follow-up checks to allow early detection
of recurrence (Roland, 2014). However, CT as well
as MRI seem to show a limited sensitivity in the
postoperative patient to diagnose recurrent disease
(Williams et al., 2003; Vercruysse et al., 2006). Also
in dogs, the only treatment for cholesteatoma is the
surgical removal of the entire epithelium (Hardie et al.,
2008). In veterinary patients, an intensive follow-up
is greatly lacking, and repeated scans are mostly
preserved for symptomatic patients only. Recurrence
is observed in 25 to 50% of the dogs diagnosed with
cholesteatoma (Little et al., 1991; Hardie et al., 2008;
Travetti et al., 2010; Greci et al., 2011).
The dog of the present case showed insidious
progressive bone destruction on repeated CT
examinations after surgical removal of a middle
ear cholesterol granuloma and cholesteatoma in the
absence of deterioration of the clinical signs.
CASE PRESENTATION
A 5.5-year old, female, intact Beagle was brought
to the referring veterinarian for a head tilt towards
the right. Two weeks previously, the owners had
noticed a sudden onset of abnormal swallowing and
a raucous coughing. The dog’s previous medical
history was unremarkable. General anesthesia was
induced to facilitate the inspection of the nasopharynx
and both ears. The eardrum was opaque and bulging
into the external ear. Following unsuccessful initial
conservative management with amoxicillin and
clavulanic acid (Synulox®, Phizer Animal Health
BV, Puurs, Belgium, 12.5 mg/kg, PO, q 12 h) in
combination with enrofloxacin (Baytril®, Bayer,
Diegem, Belgium, 5 mg/kg, PO, q 24 h), the dog
was referred to the Faculty of Veterinary Medicine of
Ghent University for a CT scan of the skull.
Both native and contrast (Omnipaque® Nycomed,
Brussels, Belgium, 300 mg I/ml, in a dosage of
1.5 ml/kg, IV, CT examinations were performed. A
single row detector spiral CT (Prospeed, GE Medical
Systems, Milwaukee, WI) was used with tube voltage
120 KvP and 100 mAs. Contiguous slices were made
from the first cervical vertebra to the cribriform plate,
perpendicular to the hard palate. Slice thickness was
3 mm, and a bone algorithm was used during survey
CT and standard algorithm during contrast CT. To
reduce partial volume artefacts, the region of interest
was re-scanned in 1mm thick slices. 2D multiplanar
reconstructed images were made in dorsal and sagittal
planes. In the initial studies, the right-sided tympanic
bulla appeared to be filled with soft-tissue density
material and showed a partially lytic ventral wall
(Figure 1). The bulla tympanica showed an abnormal
Vlaams Diergeneeskundig Tijdschrift, 2014, 83
257
Figure 1. Transverse CT pre-contrast image in bone window (A) and post-contrast image in soft tissue window (B)
before surgery show an enlarged shape of the right bulla and filling with soft-tissue density material. Partial destruction
of the ossicles (white arrowhead) and lysis at the ventral wall of the bulla can be noticed on the bone window image
(black arrow). A focal area of bone destruction is present at the petrosal portion of the temporal bone (white arrow).
The white arrows on the post-contrast image indicate enhancement of the soft tissues ventrally of the bulla.
and enlarged shape. A focal area of bone destruction
was present at the petrosal portion of the temporal
bone. The ossicles were partially destroyed. The softtissue mass extended at the level of the malleolus and
an external bulging of the tympanic membrane was
present. No abnormalities at the external ear canal
were present. In the contrast study, no abnormal
contrast medium enhancement could be noticed
intracranially or within the bulla, although there was
mild enhancement in the soft tissues ventral to it.
Based on the CT scan, the differential diagnosis was
isolated otitis media or otitis media and interna, most
likely due to cholesteatoma.
The dog was referred to the surgical department of
Small Animal Medicine of the Faculty of Veterinary
Medicine, Ghent University and scheduled for a
unilateral ventral bulla osteotomy (VBO). The ventral
wall of the bulla was grossly osteolytic and destructed,
and a sample was submitted for bacteriological
aerobic and anaerobic culture. A solitary 5x5x5 mm
brown nodule was visualized in the tympanic cavity
as well as a large amount of white pasty substance.
Both were removed and fixed separately in 10%
formalin for histopathological evaluation. After gentle
curettage, the tympanic cavity appeared to be empty
and the surgical site was copiously lavaged with warm
sterile saline and closed routinely.
The morning after surgery, the dog showed a
discrete facial nerve weakness with slow palpebral
reflex and drooping of the ipsilateral eyelid but
appeared comfortable, ate and was discharged from
the hospital. Medications were prescribed, including
the antibiotics amoxicillin and clavulanic acid (12.5
mg/kg, PO, q 12 h) and enrofloxacin (10.0 mg/kg,
PO, q 24 h) and a NSAID (meloxicam 0.1 mg/kg, PO,
Figure 2. Cholesterol granuloma, fusiform clefts (arrow)
left by cholesterol crystals, which have been dissolved
during processing. H&E, 100x. Bar = 20 µm. q 24 h) for five days. The cornea was protected by
regular application of synthetic tears.
Bacterial culturing of the intraoperative samples
yielded no growth and both of the antibiotics were
discontinued. The biopsy samples were processed
routinely and stained with HE. On microscopy, the
slides of the round, brown nodule contained large
numbers of acicular clefts, typical of cholesterol
crystals surrounded by mononuclear inflammatory
cells (mostly macrophages), giant cells and some
fibroblasts (Figure 2). Cholesterol granuloma was
diagnosed. The samples of the pasty material showed
broad acellular fibres on microscopic examination.
These were keratin fibres, confirmed by positive
cytokeratin staining (Figure 3). None of the submitted
258
Figure 3. Acellular keratinous material. Cytokeratin
stain, 200x. Bar = 20 µm.
samples contained epithelium. Nevertheless, the
presumptive diagnosis of cholesteatoma was made.
The dog’s clinical signs fully resolved within the
next two weeks. However, a head tilt towards the
right re-appeared eight months postoperatively. The
referring veterinarian diagnosed bilateral Malassezia
otitis and instituted a topical treatment with nystatinneomycin triamcinolone acetonide ointment once
daily for two weeks. The head tilt did not alter by
this treatment and a re-examination CT scan was
scheduled nine months after VBO surgery, using the
same imaging protocol as before. Slight extension
of soft-tissue material in the distal external ear canal
and expanded lysis of the tympanic wall could be
appreciated (Figure 4). Sequels of the VBO appeared
present as the absence of a large part of the ventral
and medial wall of the bulla. There was increased
lysis of the petrosal part of the temporal bone, and
Vlaams Diergeneeskundig Tijdschrift, 2014, 83
the ossicles seemed to be destroyed. The tympanic
membrane seemed to be intact. The bulla was
completely filled with a soft tissue attenuating mass
slightly enhancing after IV contrast administration.
Intravenous contrast showed rim enhancement of the
soft-tissue mass extending intracranial at the level of
the cerebellum. Because of the extension towards the
brain, a new surgical approach carried an unjustified
iatrogenic risk.
Two years after the second CT examination, i.e. 33
months after VBO surgery, the dog was represented
at the authors’ request to assess the progression of
the bony destructive lesions and the expansion of the
disease by a follow-up CT scan. There was a slight
increase of lysis at the petrosal portion of the temporal
bone compared to the previous study (Figure 5). Again,
the soft tissue mass in the bulla enhanced mildly
after IV injection of contrast medium. Moreover, the
margins of the intracranial extension of the soft-tissue
mass enhanced after IV contrast. Enhancement of the
meninges as is encountered in case of meningitis,
could not be noticed on the IV contrast images. In
contrast to the extent and the progression of the
changes seen on CT, the dog was clinically healthy
apart from a discrete and stable residual head tilt. The
owners declined further MRI examinations proposed
to assess the intracranial extension of the lesion.
The dog was rechecked clinically and continued
to have excellent clinical function 48 months after the
VBO.
DISCUSSION
An adult dog surgically treated for middle ear cholesterol granuloma and cholesteatoma was represented
twice for follow-up CT scans. Progressive lesions were
Figure 4. The native CT study (A) nine months after surgery shows an increased lysis of the petrosal part of the
temporal bone and the ossicles seem to be destroyed (white arrow). IV contrast (B) shows rim enhancement of the
soft-tissue mass extending intracranially at the level of the cerebellum (black arrow).
Vlaams Diergeneeskundig Tijdschrift, 2014, 83
visible at both occasions and a prominent intracranial
involvement was demonstrated, although the dog only
had a mild and stable head tilt.
Computed tomographic scanning is a useful
imaging modality for the detection and for the extension
of middle ear pathologies and possible associated
bony lysis in dogs (Love et al., 1995; Rohleder et
al., 2006; Travetti et al., 2010). It provides excellent
anatomical detail and the relationship between the
mass and contiguous structures, allowing a better
treatment and prognosis. Evaluating the images on
bone window and soft-tissue window is necessary
to define the complete extension. The use of small
CT slice thickness decreases the incidence of partial
volume artefacts, which occur in the tympanic region
of companion animals (Barthez et al., 1996; Garosi
et al., 2003). According to a relatively recent report
on CT features in dogs affected by cholesteatoma,
there is no appreciable contrast medium enhancement
in the tympanic bulla, although occasionally, ring
enhancement can be appreciated (Travetti et al. 2010).
However, in another report, heterogenous contrast
medium enhancement was observed in the majority
of the patients. It was interpreted as increased
vascularity in the abnormal metabolically active
squamous epithelium, surrounding the keratin debris
(Hardie et al., 2008). The appreciated changes, such
as a lytic bulla, a soft tissue-like opacity in the bulla
and a sclerotic or lytic aspect of the petrosal portion
of the temporal bone are amongst the clinical features
of cases of aural cholesteatoma (Hardie et al., 2008;
Travetti et al., 2010) but potentially also of aural
cholesterol granuloma (Fliegner et al., 2007; Riedinger
et al., 2012). The final diagnosis and differentiation
between cholesterol granuloma and cholesteatoma
can only be made by histopathologic evaluation of
the middle ear contents. In the present case, a firm
nodule (cholesterol granuloma) was removed as well
259
as pasty substance (no discrete mass) that was readily
encountered after entering the bulla (keratin debris).
Also four dogs in a previous case series of eleven
cholesteatoma patients demonstrated the contemporary
presence of cholesteatoma and multiple cholesterol
granulomas (Banco et al., 2014). The cholesterol
clefts surrounded by granulation tissue are easily
recognized as cholesterol granuloma (Cox and PayneJohnson, 1995), whereas in the classical description
of cholesteatoma, a keratinizing stratified squamous
epithelium is shedding keratin into the lumen of a
cyst (Little et al., 1991; Davidson et al., 1997). It is
not unusual for human pathologists to receive middle
ear samples obtained for histopathologic examination
that only contain keratin. Notwithstanding the lack
of epithelium, those cases are diagnosed as being
‘compatible with cholesteatoma’ since no apparent
differential diagnosis exists (personal communication
L. Stessens). Whereas the routine HE staining might
be misleading, e.g. in case of the presence of fibrin
after hemorrhage, immunohistochemistry (cytokeratin
staining) confirms the presence of keratin. Also in the
present case, a squamous epithelial lining could not
be identified in the submitted samples. Very recently,
it has been documented that the cytokine pattern of
expression in epithelium obtained from within the
tympanic bulla cannot be used as a histological feature
to suggest the cholesteatoma origin of the middle ear
pathology in dogs (Banco et al., 2014). On the other
hand, epithelial hyperplasia in the absence of adnexa
is highly suggestive of the presence of cholesteatoma
(Banco et al., 2014).
After VBO, the tympanic cavity heals by ingrowth
of granulation tissue and an obliterating proliferative
bony response (Mc Anulty et al., 1995) or by a partial
or complete bulla reformation (Holt and Walker,
1997). During the follow-up CT examinations in the
present report, refilling of the bulla and progressive
Figure 5. The bone window CT image (A), two years and nine months after surgery present a slight increase of lysis
at the petrosal portion of the temporal bone (white arrow). The wall of the intracranial extension (black arrow) of the
soft-tissue mass enhances well after IV contrast (B).
260
bone resorption were appreciated. Soft-tissue opacity
within the tympanic bulla may be attributable to the
presence of fluid or soft tissue-like material, such
as recurrent cholesteatoma, granulation tissue or
fibrous scar tissue, or mucosal edema. Computed
tomographic density measurements are of little use
because the values of Hounsfield units are similar in
all those conditions (Gotthelf, 2004). Nevertheless,
this differentiation is important since the appropriate
therapy may vary from supportive measures to
follow-up surgery. Although antibiotic treatment
is rarely effective in resolving recurrent middle ear
infection after previous surgery (Smeak et al., 1996),
controlling inflammation and infection by sustained
antibiotic therapy might limit the clinical signs in dogs
with recurrent cholesteatoma (Hardie et al., 2008). In
the dog described, no medical treatment was installed
in the later postoperative phase.
Several studies have evaluated the role of MRI in
the differentiation of granulation tissue from recurrent
cholesteatoma in human patients who had middle
ear surgery. The use of delayed contrast-enhanced
T1-weighted imaging is beneficial (Williams et al.,
2003) in differentiating non-enhancing, avascular
cholesteatoma from slowly enhancing inflammatory
and scar tissue in postoperative recidivism. Differentiation is made based on the different enhancement
patterns in relation to the time period after contrast
administration. In one of the canine cases of
cholesteatoma, in which the MRI findings have been
described in detail, some partial enhancement of the
inner lining of the bulla was observed on the postcontrast T1-weighted images (Harran et al., 2012).
According to the authors, the enhancement following
contrast administration suggest the presence of
inflammation in conjunction with the presence of the
cholesteatoma.
More recently, in a number of human reports, the
value of diffusion-weighted (DW) MRI as an accurate
method for the evaluation of intracranial disease
processes has been discussed. The method has been
shown to be accurate in differentiating inflammatory
tissue from cholesteatoma in the non-surgically
treated middle ear, as cholesteatoma demonstrates a
clear hyperintensity on DW sequences in contrast to
inflammatory tissue (Vercruysse et al., 2006; De Foer
et al., 2007), especially when used in conjunction with
standard MRI sequences (Vercruysse et al., 2006).
In the dog reported here, with DW MRI, it would
probably have been possible to accurately differentiate
inflammatory tissue from cholesteatoma but the
equipment is currently not available for veterinary use
in Belgium. To the authors’ best knowledge, the use
of DW MRI to assess pathology of the middle ear has
even not yet been described in animals.
It is very striking that the clinical condition of
the dog of the present case was not deteriorating by
the time of writing, more than four years after the
surgery, notwithstanding the progressive destructive
Vlaams Diergeneeskundig Tijdschrift, 2014, 83
lesions on the CT images. The progressive bone
resorption did not only seem to affect the tympanic
portion of the temporal bone but also the petrosal
portion of the temporal bone, suggesting intracranial
extension of the disease process. Surprisingly,
symptoms compatible with intracranial involvement,
such as central vestibular syndrome, abnormal gait,
seizures, altered mentation or cranial nerve deficits
(Sturges et al., 2006) were lacking in this dog and,
moreover, chronic intermittent systemic antibiotic
therapy was not required to keep the dog clinically
stable. Previous studies on otogenic intracranial
spread of middle ear infection showed obvious central
disease in all affected dogs that arose from the spaceoccupying nature of the lesions and/or resulted from
inflammation or edema of the brain parenchyma
(Spangler and Dewey, 2000; Sturges et al., 2006).
Also in humans, the potential for causing central
nervous system complications makes cholesteatoma
a potentially fatal lesion if infection is involved
(Roland, 2014). In the case series of Hardie et al.
(2008), there was one dog readmitted postoperatively
with lysis of the petrosal portion of the temporal bone
into the cranial fossa in the absence of signs of central
neurologic disease. It is not clear why that particular
dog as well as the dog described in this case report did
not show more severe neurological symptoms despite
the marked intracranial involvement.
In dogs with chronic middle ear disease, CT is
a valuable modality to assess the presence of bony
involvement. The contents of the tympanic bulla that
is removed at the time of surgery, should be submitted
for histopathological evaluation to differentiate
between cholesterol granuloma, cholesteatoma,
abscedation or neoplastic disease. Following surgery,
it is not yet feasible in dogs to differentiate between
recurrence and inflammatory or scar tissue formation.
More cholesteatoma cases should have an extended
follow-up, using CT or MRI to assess whether the
dry keratin formed in cases of cholesteatoma (as long
as it does not get secondarily infected) gives rise to
less clinical signs than when a lot of inflammatory
mediators are released.
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